A meta‐analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery’s rule

Abstract 1. In ant social parasitism, the process by which parasite–host systems evolved and the types of invasion mechanisms parasites use are being debated. Emery’s rule, for example, states that social parasites are the closest relatives to their hosts. The present study uses previously published data to test whether Emery’s rule applies equally to all parasitism types (i.e. xenobiosis, temporary, dulosis, and inquilinism). In addition, this study also investigates other links between parasite–host relatedness and host biology, which has implications for understanding the invasion mechanisms used by certain parasites. 2. We find that xenobiotic parasites typically use distantly‐related host species that are of at least medium colony size. Temporary parasites often have multiple host species that are very closely related to the parasite and hosts with medium‐size colonies. Dulotic parasites frequently have multiple host species that are slightly less related and of any size. Lastly, inquiline parasites tend to have a single, very closely related, host species with medium‐size colonies. 3. Parasites tend to be more closely related to host species if they have a single host species or when the host has a large colony size. In contrast, parasites with multiple host species or hosts of small colony size tend to be less related to their hosts. 4. This study is the first to examine trends in ant social parasitism across all known parasite species. Our meta‐analysis shows that Emery’s rule applies to inquilinism and temporary parasitism, but not to dulosis and xenobiosis. Our results also suggest that both parasitism type and parasite–host relatedness predict the number of hosts and host colony size. It may be that a chemical mimicry mechanism allows invasion of large host colonies, but requires close relatedness of parasite and host, and concentration on a single host species.     

The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.     

Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus

Slave-making ants are social parasites which exploit the workforce of heterospecific slaves for their own reproduction, and to this end they have developed a variety of morphological and behavioural adaptations. Furthermore, social parasites utilize the chemical communication system of their hosts by breaking their nestmate recognition code, and some slave-maker species additionally employ semiochemicals as weapons during colony foundation and slaveraiding. Here, we demonstrate the use of such a ‘propaganda allomone’ by the North American myrmicine slave-maker Protomognathus americanus. This substance is produced in the Dufour’s gland and may be employed during slave raids to elicit panic among defending host workers. Slave-maker Dufour’s gland secretions evoked agitation and heightened levels of activity among host workers when applied directly on a host nest, and strong aggressive responses of nestmates when applied onto a host worker. Although the hosts own Dufour’s gland secretion also elicits intra-colonial fights, no support for the hypothesis was found that the slave-maker propaganda substance mimics a fertility signal of the host, as the chemical profile of the gland secretions is highly divergent between the two species. Preliminary results on the chemical composition of the secretion obtained by gas chromatography indicate that the propaganda substance of P. americanus differs from that of the related European slavemaker Harpagoxenus sublaevis, and is thus likely to represent an independent evolutionary development. Received 24 February 2005; revised 28 July 2005 and 2 March 2006; accepted 6 March 2006.     

Body size changes among otters, Lutra lutra, in Norway: the possible effects of food availability and global warming

Using museum data of adult specimens whose sex, age, and locality are known, we studied temporal and geographical body size trends among the otter, Lutra lutra, in Norway. We found that body size of the otters increased during the last quarter of the twentieth century, and suggest that this trend is related to increased food availability from fish farming and possibly also to energy saving due to elevated sea temperatures. Birth year and death year explained 38.8 and 43.5%, respectively, of the variation in body size. Body size of otters was positively related to latitude, thus conforming to Bergmann’s rule.     

The ecological success of a social parasite increases with manipulation of collective host behaviour

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite‐induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour‐treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker‐induced nestmate attack. Slavemakers benefited from altering their hosts’ aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker‐induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T. curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T. longispinosus. Our findings highlight that large‐scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.     

Local host ant specificity of Phengaris (Maculinea) teleius butterfly,an obligatory social parasite of Myrmica ants

1. Phengaris butterflies are obligatory social parasites of Myrmica ants. Early research suggested that there is a different Myrmica host species for each of the five European Phengaris social parasites, but more recent studies have shown that this was an oversimplification. 2. The pattern of host ant specificity within a Phengaris teleius metapopulation from southern Poland is reported. A combination of studying the frequency distribution of Phengaris occurrence and morphometrics on adult butterflies were used to test whether use of different host species is reflected in larval development. 3. Phengaris teleius larvae were found to survive in colonies of four Myrmica species: M. scabrinodis, M. rubra, M. ruginodis, and M. rugulosa. Myrmica scabrinodis was the most abundant species under the host plant but the percentage of infested nests was similar to other host ant species at two sites and lower in comparison to nests of M. rubra and M. ruginodis at the other two sites. Morphometric measurements of adult butterflies reared by wild colonies of M. scabrinodis and M. ruginodis showed that wing size and number of wing spots were slightly greater for adults eclosing from nests of M. ruginodis. 4. Our results suggest that P. teleius in the populations studied is less specialised than previously suggested. The results are consistent with the hypothesis that P. teleius is expected to be the least specific of the European Phengaris species, as it has the largest and best defended fourth‐instar caterpillars and, as a predatory species, it spends less time in the central larval chambers of the host colonies. The fact that individuals reared by M. ruginodis had wider hind wings may suggest that P. teleius had better access to resources in M. ruginodis than in M. scabrinodis colonies.     

Recommendations for the use of species diversity indices with reference to a recently published article as an example

There are some recommendations for the use of species diversity indices in a paper recently published in this journal by M. Ohsawa on the species richness and composition of weevils in five forest types in the middle region of Japan. Because several factors, such as small sample size, calculation of Simpson’s diversity index by the use of the original equation of Simpson’s measure of concentration D, and a weak point in the Shannon–Wiener diversity index H′, may have led to biased estimates, I recalculated these indices using combined species diversity values of the five forest types. As the general tendencies of 1−D and H′ values calculated here were similar to those in Ohsawa’s paper, there is no need to propose any change to his view. However, these recalculated diversity indices indicated that they are values which are more suitable for use. It should be noted that the characteristics and weak point associated with the diversity indices need to be taken into account in future studies.     

Treatment of refractory Hodgkin’s disease with an anti-CD16/CD30 bispecific antibody

 A group of 15 patients with refractory Hodgkin′s disease were treated in a phase I/II trial with the natural-killer (NK)-cell-activating bispecific monoclonal antibody HRS-3/A9, which is directed against the Fcγ receptor III (CD16 antigen) and the Hodgkin’s associated CD30 antigen. The antibody was given four times every 3 – 4 days, starting with 1 mg/m². The treatment was well tolerated and the maximum tolerated dose was not reached at 64 mg/m². Side-effects were rare and consisted of fever, pain in involved lymph nodes and a maculopapulous rash. Nine patients developed human anti-(mouse immunoglobulin) antibodies. One complete and one partial remission (lasting 5 and 3 months, respectively), three minor responses (1 to 11+ months), and one mixed response were achieved. There was no clear-cut dose side-effect or dose/response correlation. NK cell activity increased in most of the patients treated with 4 mg/m² or higher doses but lasted no longer than 6 weeks after therapy. Our results encourage further clinical trials with this novel immunotherapeutic approach and emphasize the necessity to reduce the immunogenicity of the antibody to allow retreatment of responding patients. Accepted: 14 October 1997     

Interaction of an entomopathogen with an insect social form: an epizootic of Thelohania solenopsae (Microsporidia) in a population of the red imported fire ant, Solenopsis invicta

This is the first report of Thelohania solenopsae infections in monogyne (single-queen) Solenopsis invicta colonies in the field. In a 0.2-ha plot near Baton Rouge, Louisiana, inter-colony prevalence was 63% infection in June, 1999, when the population was 100% monogyne. In February, 2000, 21% of 33 monogyne and 90% of 10 polygyne colonies were infected. By May, 2001, the polygyne colonies had disappeared and only one of 34 monogyne colonies was infected, the final detection of T. solenopsae in the plot. Colony size did not differ significantly among the four types (monogyne versus polygynexinfected versus uninfected).     

Age-related alteration of PKC, a key enzyme in memory processes

Brain aging is characterized by a progressive decline of the cognitive and memory functions. It is becoming increasingly clear that protein phosphorylation and, in particular, the activity of the calcium-phospholipid-dependent protein kinase C (PKC) may be one of the fundamental cellular changes associated with memory function. PKC is a multigene family of enzymes highly expressed in brain tissues. The activation of kinase C is coupled with its translocation from the cytosol to different intracellular sites and recent studies have demonstrated the key role played by several anchoring proteins in this mechanism. PKC-phosphorylating activity appears to be impaired during senescence at brain level in a strain-dependent fashion in rodents. Whereas the levels of the various isoforms do not show age-related alterations, the enzyme translocation upon phorbol-ester treatment is deficitary among all strains investigated. Anchoring proteins may contribute to this activation deficit. We discuss also modifications of the PKC system in Alzheimer's disease that may be related to pathological alterations in neurotransmission. A better insight of the different factors controlling brain-PKC activation may be important not only for elucidating the molecular basis of neuronal transmission, but also for identifying new approaches for correcting or even preventing age-dependent changes in brain function.     

The ecological distribution of reproductive mode in oribatid mites, as related to biological complexity

The high incidence of asexuality in oribatid mites presents an unusual opportunity for examining hypotheses for the maintenance of sex. There is a presumed range in age of asexual species: many oribatid species are phylogenetically clustered, occurring in speciose early-derivative families or genera without sexual species, while others are phylogenetically isolated from other asexual species, occurring in later derivative taxa with sexual congeners. We examined the distribution of oribatid mite reproductive mode in soil of corn fields, grassy and shrub fields, and forests in central New York State (three replicate plots of each type, with 25 samples per plot), to test three ecological predictions from current theory. (1) If overall biotic uncertainty, as generated by competitors and predators, mediates the ecological distribution of oribatid mites, then the proportion of asexual oribatid mites should be negatively correlated with biological diversity; we examine this prediction using literature data as well. (2) If Muller’s Ratchet (the stochastic loss of best genotypes, which is independent of environment), mediates the success of asexuality, then no ecological pattern should exist. (3) If general purpose genotypes are characteristic of asexual oribatid mites, their habitat distribution should be broader than that of sexual species. For each plot the level of asexuality was compared to indices of overall biotic diversity, as calculated from the pooled oribatid mite (competitors) and mesostigmatid mite (predator) communities. We found no negative correlation in this relationship in our own data or in the literature analysis of 290 faunal surveys from 50 literature sources, so we reject biotic uncertainty as an important determinant of reproductive mode distribution. When only data on phylogenetically clustered asexuals are considered, there is instead a positive correlation between asexuality and diversity that is not explained. Because of the latter pattern we tentatively reject Muller’s Ratchet as the primary factor maintaining reproductive mode in these mites, but cannot reject it for isolated asexual species. Niche breadth in sexual and asexual oribatid mites provides no support for widespread general purpose genotypes but broad patterns in the literature suggest that the idea needs further investigation. Possible complicating or unknown factors that are discussed include historical disturbance in the study area, the relationship between parasitism and general biotic diversity, and the level and source of genetic diversity in asexual oribatid mites.     

Use of desmids to assess the natural conservation value of a Hungarian oxbow (Malom-Tisza,NE-Hungary)

A method recently proposed by Coesel that uses the desmid flora to assess the conservation value of aquatic habitats was applied to an alkaline and hypertrophic oxbow of the Upper Tisza river (NE Hungary). According to the macrophyte community the oxbow contains two distinct habitats, both of which provide suitable conditions for the development of a rich desmid flora. High temporal and spatial differences in the algal flora were observed in periphyton and plankton samples taken in June and August 2004. The sample of Utricularia vulgaris periphyton collected in August was characterised by the most species-rich desmid flora. The conservation value of this sample was the maximum according to Coesel’s method. The latter also proved to be useful for the assessment of the conservation value of plankton net samples taken from among the macrophytes. The use of modified rarity value calculations as recently proposed by Fehér did not significantly affect the conservation value, but different enumeration methods to quantify the floristic diversity did result in different conservation values. We found that Coesel’s desmid based method is a useful tool for assessing the conservation value of the studied oxbow. Based our results the Coesel method’s applicability and usefulness depended on (i) the sampling location (open water or macrophytic region) samples were taken from open water or from macrophytic region; and (ii) species enumeration procedures (up to 400 specimens counted, or whole droplets counted). Presented at the International Symposium Biology and Taxonomy of Green Algae V, Smolenice, June 26–29, 2007, Slovakia.     

Breeding ecology of an Old World high-altitude warbler, Phylloscopus affinis

Reproduction of Tickell’s Leaf Warblers Phylloscopus affinis was studied in an alpine valley (29°27′N, 91°40′E, 3,980–5,600 m) in the Lhasa mountains, Tibet, at the upper elevational limit of the species’ breeding range. This species is a summer breeder, and is the only breeding Phylloscopus species in the valley. It nested in all types of shrubby vegetation across the altitudinal range of the valley. Most nests were placed close to the ground (<1 m) in low thorn bushes. Egg-laying dates fell between late May and early July, most within the first 3 weeks after the commencement of breeding. Mean clutch size was 4.0 (3–5) and mean brood size at fledging 3.4 (2–5). Incubation was by the females and lasted 13–14 days, and both parents cared for the young for 14–17 days. Nestlings ready to leave the nest were 13% heavier than the adults. Overall, 76% of nesting attempts produced at least one fledged young. Some aspects of the breeding biology of this high-altitude warbler were compared with those of lower-altitude Phylloscopus species.     

The molecular basis of speciation: from patterns to processes,rules to mechanisms

The empirical study of speciation has brought us closer to unlocking the origins of life’s vast diversity. By examining recently formed species, a number of general patterns, or rules, become apparent. Among fixed differences between species, sexual genes and traits are one of the most rapidly evolving and novel functional classes, and premating isolation often develops earlier than postmating isolation. Among interspecific hybrids, sterility evolves faster than inviability, the X-chromosome has a greater effect on incompatibilities than autosomes, and hybrid dysfunction affects the heterogametic sex more frequently than the homogametic sex (Haldane’s rule). Haldane’s rule, in particular, has played a major role in reviving interest in the genetics of speciation. However, the large genetic and reproductive differences between taxa and the multi-factorial nature of each rule have made it difficult to ascribe general mechanisms. Here, we review the extensive progress made since Darwin on understanding the origin of species. We revisit the rules of speciation, regarding them as landmarks as species evolve through time. We contrast these ‘rules’ of speciation to ‘mechanisms’ of speciation representing primary causal factors ranging across various levels of organization—from genic to chromosomal to organismal. To explain the rules, we propose a new ‘hierarchical faster-sex’ theory: the rapid evolution of sex and reproduction-related (SRR) genes (faster-SRR evolution), in combination with the preferential involvement of the X-chromosome (hemizygous X-effects) and sexually selected male traits (faster-male evolution). This unified theory explains a comprehensive set of speciation rules at both the prezyotic and postzygotic levels and also serves as a cohesive alternative to dominance, composite, and recent genomic conflict interpretations of Haldane’s rule.     

Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission,Aphaenogaster senilis

Abstract. 1. In eusocial insects, colony fission is a mode of dispersal by which a young queen leaves her nest with some workers to found a new colony. In these species, adult females (workers and the queen) should allocate most resources to increasing their colony size, which constrains the possibility of fission. In contrast, developing diploid larvae should have a preference for becoming a queen and having their own offspring, rather than becoming workers and rearing the offspring of other females. 2. In the ant Aphaenogaster senilis, queens are produced in very small numbers, suggesting that adult females control larval development. We used a 6‐year series of data on more than 300 nests to determine the annual cycle of worker and queen production. Although both overlapped, the latter mostly occurred in the second half of the summer, after a major peak of worker emergence. Young queens were also often produced in nests whose reproductive queen had died, thus allowing her replacement. Overall, we estimate that only 0.07% of diploid larvae actually develop into gynes. 3. Laboratory experiments indicated that brood is bipotent until the second larval instar. Diploid larval development into queen was favoured by the removal of the mother queen, but was not affected by rearing temperature. 4. Our data suggest that most diploid broods are forced by the adults to develop into workers rather than into gynes. However, when the queen is not present due to death or after a fission event, a few larvae are allowed to develop into gynes. One way for workers to limit the development of larvae might be by controlling the amount of food they receive.     

Biology of a new species of socially parasitic thrips (Thysanoptera: Phlaeothripidae) inside Dunatothrips nests,with evolutionary implications for inquilinism in thrips

Akainothrips francisi sp. nov. is shown to be an inquiline (i.e. it invades, and breeds within, domiciles of another species). Currently, its only known host is Dunatothrips aneurae, a subsocial thrips that creates silken domiciles by securing together phyllodes of mulga (Acacia aneura) in the arid zone of Australia. We found Ak. francisi prolifically breeding inside live D. aneurae host domiciles, both immature and mature. Akainothrips francisi did not kill its host and we saw no evidence of antagonistic host‐inquiline interactions. This is thus the second demonstrably inquiline species of Acacia thrips, although other possible inquilines have been suggested including two Akainothrips. We found that Ak. francisi occurred with positive density dependence, and was associated with moderately reduced host reproduction. This latter association was especially evident in larger host domiciles, suggesting that Ak. francisi either inhibits further host reproduction after invasion or exploits poor quality hosts more successfully. Sex ratios were slightly female biased. Akainothrips francisi males were exceptionally variable in size, colour, and foreleg size compared to females, with morphs co‐occurring within domiciles, suggesting sexual selection and the possibility of different male reproductive strategies. The discovery of Ak. francisi highlights particular morphological affinities among known or suspected inquiline Acacia thrips within Akainothrips and other genera, allowing us to hypothesize a common origin of this lifestyle from within Akainothrips. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Mechanism of DNA Damage and Apoptosis Induced by Tetrahydropapaveroline, a Metabolite of Dopamine

Tetrahydropapaveroline (THP), a metabolite of dopamine, has been suspected to be associated with dopaminergic neurotoxicity of L-DOPA. THP induced apoptosis in human leukemia cell line HL-60 cells, but did not in its hydrogen peroxide (H₂O₂)-resistant clone HP100. THP-induced DNA ladder formation in HL-60 cells was inhibited by a metal chelator. THP induced damage to ³²P-labeled DNA fragments in the presence of metals. In the presence of Fe(III)EDTA, THP caused DNA damage at every nucleotide. The DNA damage was inhibited by free hydroxy radical (^·OH) scavengers and catalase, suggesting that the Fe(III)EDTA-mediated DNA damage is mainly due to ^·OH generation. In the presence of Cu(II), THP caused DNA damage mainly at T and G of 5′-TG-3′ sequence. The inhibitive effect of catalase and bathocuproine on Cu(II)-mediated DNA damage suggested that H₂O₂ and Cu(I) participate in the DNA damage. This study demonstrated that THP-induced apoptosis via reactive oxygen species generated from reaction of H₂O₂ and metals plays an important role in cytotoxicity of L-DOPA.